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As the core of heterosis utilization, cytoplasmic male sterility (CMS) has been widely used in hybrid seed production. Previous studies have shown that CMS is always closely related to the altered programming of mitochondrial genes. To explore candidate CMS genes in cotton (<i>Gossypium hirsutum</i>), sequencing and de novo assembly were performed on the mitochondrial genome of the <i>G. hirsutum</i> CMS line SI3A, with <i>G. harknessii</i> CMS-D2 cytoplasm, and the corresponding <i>G. hirsutum</i> restorer line 0-613-2R. Remarkable variations in genome structure and gene transcripts were detected. The mitochondrial genome of SI3A has three circle molecules, including one main circle and two sub-circles, while 0-613-2R only has one. RNA-seq and RT-qPCR analysis proved that <i>orf606a</i> and <i>orf109a</i>, which have a chimeric structure and transmembrane domain, were highly expressed in abortive anthers of SI3A. In addition, comparative analysis of RNA-seq and full-length transcripts revealed the complex I gene <i>nad4</i> to be expressed at a lower level in SI3A than in its restorer and that it featured an intron retention splicing pattern. These two novel chimeric ORFs and <i>nad4</i> are potential candidates that confer CMS character in SI3A. This study provides new insight into the molecular basis of the nuclear–cytoplasmic interaction mechanism, and that putative CMS genes might be important sources for future precise design cross-breeding of cotton.